Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-30T07:40:55.816Z Has data issue: false hasContentIssue false
  • English
  • Français

Paper as a scaffold for cell cultures: Teaching an old material new tricks

Published online by Cambridge University Press:  24 January 2018

Xinchen Wu ,
Sanika Suvarnapathaki ,
Kierra Walsh  and
Gulden Camci-Unal
Xinchen Wu
Affiliation:
Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, One University Avenue, Lowell, MA 01854, USA
Sanika Suvarnapathaki
Affiliation:
Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, One University Avenue, Lowell, MA 01854, USA
Kierra Walsh
Affiliation:
Department of Biological Sciences, University of Massachusetts Lowell, One University Avenue, Lowell, MA 01854, USA
Gulden Camci-Unal*
Affiliation:
Department of Chemical Engineering, University of Massachusetts Lowell, One University Avenue, Lowell, MA 01854, USA
*
Address all correspondence to Gulden Camci-Unal at [email protected]
Get access

Abstract

Paper-based cell culture platforms have emerged as a promising approach for a myriad of biomedical applications, such as tissue engineering, disease models, cancer research, biotechnology, high-throughput testing, biosensing, and diagnostics. Paper enables the generation of highly flexible, biocompatible, inexpensive, porous, and three-dimensional (3D) constructs and devices. These systems have been used to culture mammalian cells, bacteria, algae, and fungi. Studies have shown that paper is an exceptional material for applications in life sciences, materials sciences, engineering, and medicine. Paper has been employed for creating biomimetic cell culture environments by folding or stacking it into the desired 3D shapes and structures. This review discusses the use of paper-based platforms for cellular applications and provides a diverse range of examples.

Type
Prospective Articles
Information
MRS Communications , Volume 8 , Issue 1 , March 2018 , pp. 1 - 14
Check for updates
Copyright
Copyright © Materials Research Society 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Jamal, M., Kadam, S.S., Xiao, R., Jivan, F., Onn, T.M., Fernandes, R., Nguyen, T.D., and Gracias, D.H.: Bio-origami hydrogel scaffolds composed of photocrosslinked PEG bilayers. Adv. Healthc. Mater. 2, 1142–1150 (2013).CrossRefGoogle ScholarPubMed
2. Peraza-Hernandez, E.A., Hartl, D.J., Malak, R.J. Jr., and Lagoudas, D.C.: Origami-inspired active structures: a synthesis and review. Smart Mater. Struct. 23, 094001 (2014).CrossRefGoogle Scholar
3. Moreau, J.E., Anderson, K., Mauney, J.R., Nguyen, T., Kaplan, D.L., and Rosenblatt, M.: Tissue-engineered bone serves as a target for metastasis of human breast cancer in a mouse model. Cancer Res. 67, 10304–10308 (2007).CrossRefGoogle ScholarPubMed
4. Derda, R., Tang, S.K., Laromaine, A., Mosadegh, B., Hong, E., Mwangi, M., Mammoto, A., Ingber, D.E., and Whitesides, G.M.: Multizone paper platform for 3D cell cultures. PLoS ONE 6, e18940 (2011).Google Scholar
5. Camci-Unal, G., Newsome, D., Eustace, B.K., and Whitesides, G.M.: Fibroblasts enhance migration of human lung cancer cells in a paper-based coculture system. Adv. Healthc. Mater. 5, 641–647 (2016).CrossRefGoogle Scholar
6. Camci-Unal, G., Laromaine, A., Hong, E., Derda, R., and Whitesides, G.M.: Biomineralization guided by paper templates. Sci. Rep. 6, 27693 (2016).CrossRefGoogle ScholarPubMed
7. Piraino, F., Camci-Unal, G., Hancock, M.J., Rasponi, M., and Khademhosseini, A.: Multi-gradient hydrogels produced layer by layer with capillary flow and crosslinking in open microchannels. Lab. Chip 12, 659–661 (2012).CrossRefGoogle ScholarPubMed
8. Hancock, M.J., Piraino, F., Camci-Unal, G., Rasponi, M., and Khademhosseini, A.: Anisotropic material synthesis by capillary flow in a fluid stripe. Biomaterials 32, 6493–6504 (2011).CrossRefGoogle Scholar
9. Hjortnaes, J., Camci-Unal, G., Hutcheson, J.D., Jung, S.M., Schoen, F.J., Kluin, J., Aikawa, E., and Khademhosseini, A.: Directing valvular interstitial cell myofibroblast-like differentiation in a hybrid hydrogel platform. Adv. Healthc. Mater. 4, 121–130 (2015).CrossRefGoogle Scholar
10. Hsieh, H.-Y., Camci-Unal, G., Huang, T.-W., Liao, R., Chen, T.-J., Paul, A., Tseng, F.-G., and Khademhosseini, A.: Gradient static-strain stimulation in a microfluidic chip for 3D cellular alignment. Lab. Chip 14, 482–493 (2014).Google Scholar
11. Lantigua, D., Kelly, Y.N., Unal, B., and Camci-Unal, G.: Engineered paper-based cell culture platforms. Adv. Healthc. Mater. 6, 22 (2017).CrossRefGoogle ScholarPubMed
12. Sapp, M.C., Fares, H.J., Estrada, A.C., and Grande-Allen, K.J.: Multilayer three-dimensional filter paper constructs for the culture and analysis of aortic valvular interstitial cells. Acta Biomater. 13, 199–206 (2015).CrossRefGoogle ScholarPubMed
13. Ng, K., Gao, B., Yong, K.W., Li, Y., Shi, M., Zhao, X., Li, Z., Zhang, X., Pingguan-Murphy, B., Yang, H., and Xu, F.: Paper-based cell culture platform and its emerging biomedical applications. Mater. Today 20, 32–44 (2017).Google Scholar
14. Freed, L.E., Vunjak-Novakovic, G., Biron, R.J., Eagles, D.B., Lesnoy, D.C., Barlow, S.K., and Langer, R.: Biodegradable polymer scaffolds for tissue engineering. Nat. Biotechnol. 12, 689–693 (1994).Google Scholar
15. Chan, C.Y., Huang, P.-H., Guo, F., Ding, X., Kapur, V., Mai, J.D., Yuen, P.K., and Huang, T.J.: Accelerating drug discovery via organs-on-chips. Lab. Chip 13, 4697–4710 (2013).CrossRefGoogle ScholarPubMed
16. Park, H.-J., Yu, S.J., Yang, K., Jin, Y., Cho, A.-N., Kim, J., Lee, B., Yang, H.S., Im, S.G., and Cho, S.-W.: based bioactive scaffolds for stem cell-mediated bone tissue engineering. Biomaterials 35, 9811–9823 (2014).Google Scholar
17. Wang, Y., Uemura, T., Dong, J., Kojima, H., Tanaka, J., and Tateishi, T.: Application of perfusion culture system improves in vitro and in vivo osteogenesis of bone marrow-derived osteoblastic cells in porous ceramic materials. Tissue Eng. 9, 1205–1214 (2003).Google Scholar
18. Agarwal, R. and García, A.J.: Biomaterial strategies for engineering implants for enhanced osseointegration and bone repair. Adv. Drug Deliv. Rev. 94, 53–62 (2015).CrossRefGoogle ScholarPubMed
19. Derda, R., Laromaine, A., Mammoto, A., Tang, S.K., Mammoto, T., Ingber, D.E., and Whitesides, G.M.: Supported 3D cell culture for tissue-based bioassays. Proc. Natl. Acad. Sci. USA 106, 18457–18462 (2009).Google Scholar
20. Mosadegh, B., Dabiri, B.E., Lockett, M.R., Derda, R., Campbell, P., Parker, K.K., and Whitesides, G.M.: Three-dimensional paper-based model for cardiac ischemia. Adv. Healthc. Mater. 3, 1036–1043 (2014).CrossRefGoogle ScholarPubMed
21. Wang, L., Xu, C., Zhu, Y., Yu, Y., Sun, N., Zhang, X., Feng, K., and Qin, J.: Human induced pluripotent stem cell-derived beating cardiac tissues on paper. Lab. Chip 15, 4283–4290 (2015).CrossRefGoogle ScholarPubMed
22. GE Lifesciences: https://www.gelifesciences.com/ (accessed 12/2/2017).Google Scholar
23. Mosadegh, B., Lockett, M.R., Minn, K.T., Simon, K.A., Gilbert, K., Hillier, S., Newsome, D., Li, H., Hall, A.B., and Boucher, D.M.: A paper-based invasion assay: Assessing chemotaxis of cancer cells in gradients of oxygen. Biomaterials 52, 262–271 (2015).CrossRefGoogle ScholarPubMed
24. Choi, G., Hassett, D.J., and Choi, S.: A paper-based microbial fuel cell array for rapid and high-throughput screening of electricity-producing bacteria. Analyst 140, 4277–4283 (2015).Google Scholar
25. Fraiwan, A., Mukherjee, S., Sundermier, S., Lee, H.-S., and Choi, S.: A paper-based microbial fuel cell: Instant battery for disposable diagnostic devices. Biosens. Bioelectron. 49, 410–414 (2013).Google Scholar
26. Martins, N.C., Freire, C.S., Neto, C.P., Silvestre, A.J., Causio, J., Baldi, G., Sadocco, P., and Trindade, T.: Antibacterial paper based on composite coatings of nanofibrillated cellulose and ZnO. Colloids Surf. A 417, 111–119 (2013).CrossRefGoogle Scholar
27. Funes-Huacca, M., Wu, A., Szepesvari, E., Rajendran, P., Kwan-Wong, N., Razgulin, A., Shen, Y., Kagira, J., Campbell, R., and Derda, R.: Portable self-contained cultures for phage and bacteria made of paper and tape. Lab Chip 12, 4269–4278 (2012).CrossRefGoogle ScholarPubMed
28. Deiss, F., Funes-Huacca, M.E., Bal, J., Tjhung, K.F., and Derda, R.: Antimicrobial susceptibility assays in paper-based portable culture devices. Lab Chip 14, 167–171 (2014).CrossRefGoogle ScholarPubMed
29. Stielow, J.B., Vaas, L.A., Göker, M., Hoffmann, P., and Klenk, H.-P.: Charcoal filter paper improves the viability of cryopreserved filamentous ectomycorrhizal and saprotrophic Basidiomycota and Ascomycota. Mycologia 104, 324–330 (2012).CrossRefGoogle ScholarPubMed
30. Chen, C.-C., Liu, Y.-J., and Yao, D.-J.: Paper-based device for separation and cultivation of single microalga. Talanta 145, 60–65 (2015).CrossRefGoogle ScholarPubMed
31. Bhattacharya, I., Ghayor, C., and Weber, F.E.: The use of adipose tissue-derived progenitors in bone tissue engineering-a review. Transfus. Med. Hemother. 43, 336–343 (2016).Google Scholar
32. Petersen, G.F., Hilbert, B.J., Trope, G.D., Kalle, W.H., and Strappe, P.M.: A paper-based scaffold for enhanced osteogenic differentiation of equine adipose-derived stem cells. Biotechnol. Lett. 37, 2321–2331 (2015).Google Scholar
33. Patnaik, J.L., Byers, T., DiGuiseppi, C., Dabelea, D., and Denberg, T.D.: Cardiovascular disease competes with breast cancer as the leading cause of death for older females diagnosed with breast cancer: a retrospective cohort study. Breast Cancer Res. 13, R64 (2011).Google Scholar
34. Petsche Connell, J., Camci-Unal, G., Khademhosseini, A., and Jacot, J.G.: Amniotic fluid-derived stem cells for cardiovascular tissue engineering applications. Tissue Eng. Part B Rev. 19, 368–379 (2013).CrossRefGoogle ScholarPubMed
35. Camci-Unal, G., Alemdar, N., Annabi, N., and Khademhosseini, A.: Oxygen-releasing biomaterials for tissue engineering. ACS Biomater. Sci. Eng. 62, 843–848 (2013).Google Scholar
36. Alemdar, N., Leijten, J., Camci-Unal, G., Hjortnaes, J., Ribas, J., Paul, A., Mostafalu, P., Gaharwar, A.K., Qiu, Y., and Sonkusale, S.: Oxygen-generating photo-cross-linkable hydrogels support cardiac progenitor cell survival by reducing hypoxia-induced necrosis. ACS Biomater. Sci. Eng. 3, 9 (2016).Google ScholarPubMed
37. Lynch, H.T., Smyrk, T.C., Watson, P., Lanspa, S.J., Lynch, J.F., Lynch, P.M., Cavalieri, R.J., and Boland, C.R.: Genetics, natural history, tumor spectrum, and pathology of hereditary nonpolyposis colorectal cancer: an updated review. Gastroenterology 104, 1535–1549 (1993).Google Scholar
38. Karlsson, H., Fryknäs, M., Larsson, R., and Nygren, P.: Loss of cancer drug activity in colon cancer HCT-116 cells during spheroid formation in a new 3-D spheroid cell culture system. Exp. Cell Res. 318, 1577–1585 (2012).CrossRefGoogle Scholar
39. Luca, A.C., Mersch, S., Deenen, R., Schmidt, S., Messner, I., Schäfer, K.-L., Baldus, S.E., Huckenbeck, W., Piekorz, R.P., and Knoefel, W.T.: Impact of the 3D microenvironment on phenotype, gene expression, and EGFR inhibition of colorectal cancer cell lines. PLoS ONE 8, e59689 (2013).CrossRefGoogle ScholarPubMed
40. Hong, B., Xue, P., Wu, Y., Bao, J., Chuah, Y.J., and Kang, Y.: A concentration gradient generator on a paper-based microfluidic chip coupled with cell culture microarray for high-throughput drug screening. Biomed. Microdevices 18, 21 (2016).CrossRefGoogle ScholarPubMed
41. Wang, S., Ge, L., Song, X., Yu, J., Ge, S., Huang, J., and Zeng, F.: based chemiluminescence ELISA: lab-on-paper based on chitosan modified paper device and wax-screen-printing. Biosens. Bioelectron. 31, 212–218 (2012).CrossRefGoogle ScholarPubMed
42. Erickson, K., Braun, R.D., Yu, D., Lanzen, J., Wilson, D., Brizel, D.M., Secomb, T.W., Biaglow, J.E., and Dewhirst, M.W.: Effect of longitudinal oxygen gradients on effectiveness of manipulation of tumor oxygenation. Cancer Res. 63, 4705–4712 (2003).Google Scholar
43. Han, T., Kang, D., Ji, D., Wang, X., Zhan, W., Fu, M., Xin, H.-B., and Wang, J.-B.: How does cancer cell metabolism affect tumor migration and invasion? Cell Adh. Migr. 7, 395–403 (2013).Google Scholar
44. Cristini, V., Frieboes, H.B., Gatenby, R., Caserta, S., Ferrari, M., and Sinek, J.: Morphologic instability and cancer invasion. Clin. Cancer Res. 11, 6772–6779 (2005).Google Scholar
45. Carmona-Fontaine, C., Bucci, V., Akkari, L., Deforet, M., Joyce, J.A., and Xavier, J.B.: Emergence of spatial structure in the tumor microenvironment due to the Warburg effect. Proc. Natl. Acad. Sci. USA 110, 19402–19407 (2013).Google Scholar
46. Boyce, M.W., LaBonia, G.J., Hummon, A.B., and Lockett, M.R.: Assessing chemotherapeutic effectiveness using a paper-based tumor model. Analyst 142, 2819–2827 (2017).Google Scholar
47. Boyce, M.W., Kenney, R.M., Truong, A.S., and Lockett, M.R.: Quantifying oxygen in paper-based cell cultures with luminescent thin film sensors. Anal. Bioanal. Chem. 408, 2985–2992 (2016).CrossRefGoogle ScholarPubMed
48. Chwalek, K., Bray, L.J., and Werner, C.: Tissue-engineered 3D tumor angiogenesis models: potential technologies for anti-cancer drug discovery. Adv. Drug Deliv. Rev. 79, 30–39 (2014).CrossRefGoogle ScholarPubMed
49. Lei, K.F., and Huang, C.-H.: Based microreactor integrating cell culture and subsequent immunoassay for the investigation of cellular phosphorylation. ACS Appl. Mater. Interfaces 6, 22423–22429 (2014).Google Scholar
50. Truong, A.S., Lochbaum, C.A., Boyce, M.W., and Lockett, M.R.: Tracking the invasion of small numbers of cells in paper-based assays with quantitative PCR. Anal. Chem. 87, 11263–11270 (2015).CrossRefGoogle ScholarPubMed
51. Zhang, J. and Liu, J.: Tumor stroma as targets for cancer therapy. Pharmacol. Ther. 137, 200–215 (2013).Google Scholar
52. Bremnes, R.M., Dønnem, T., Al-Saad, S., Al-Shibli, K., Andersen, S., Sirera, R., Camps, C., Marinez, I., and Busund, L.-T.: The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. J. Thorac. Oncol. 6, 209–217 (2011).CrossRefGoogle ScholarPubMed
53. Deiss, F., Mazzeo, A., Hong, E., Ingber, D.E., Derda, R., and Whitesides, G.M.: Platform for high-throughput testing of the effect of soluble compounds on 3D cell cultures. Anal. Chem. 85, 8085–8094 (2013).Google Scholar
54. Deiss, F., Matochko, W.L., Govindasamy, N., Lin, E.Y., and Derda, R.: Flow-through synthesis on teflon-patterned paper to produce peptide arrays for cell-based assays. Angew. Chem. Int. Ed. 53, 6374–6377 (2014).Google Scholar
55. Jackson, S.P., and Bartek, J.: The DNA-damage response in human biology and disease. Nature 461, 1071 (2009).CrossRefGoogle ScholarPubMed
56. Begg, A.C., Stewart, F.A., and Vens, C.: Strategies to improve radiotherapy with targeted drugs. Nat. Rev. Cancer 11, 239 (2011).Google Scholar
57. Barnett, G.C., West, C.M., Dunning, A.M., Elliott, R.M., Coles, C.E., Pharoah, P.D., and Burnet, N.G.: Normal tissue reactions to radiotherapy: towards tailoring treatment dose by genotype. Nat. Rev. Cancer 9, 134 (2009).Google Scholar
58. Simon, K.A., Mosadegh, B., Minn, K.T., Lockett, M.R., Mohammady, M.R., Boucher, D.M., Hall, A.B., Hillier, S.M., Udagawa, T., Eustace, B.K., and Whitesides, G.M.: Metabolic response of lung cancer cells to radiation in a paper-based 3D cell culture system. Biomaterials 95, 47–59 (2016).Google Scholar
59. Kenney, R.M., Boyce, M.W., Truong, A.S., Bagnell, C.R., and Lockett, M.R.: Real-time imaging of cancer cell chemotaxis in paper-based scaffolds. Analyst 141, 661–668 (2016).CrossRefGoogle ScholarPubMed
60. Tao, F.F., Xiao, X., Lei, K.F., and Lee, I.-C.: Based cell culture microfluidic system. Biochip J. 2, 97–104 (2015).Google Scholar
61. Lei, K.F., Huang, C.-H., and Tsang, N.-M.: Impedimetric quantification of cells encapsulated in hydrogel cultured in a paper-based microchamber. Talanta 147, 628–633 (2016).CrossRefGoogle Scholar
62. Choi, G. and Choi, S.: Bacterial cell transportation in paper-based microfluidics. In Transducers (IEEE: Anchorage, Alaska, USA, 2015), pp. 1921–1924.Google Scholar
63. Yetisen, A.K., Akram, M.S., and Lowe, C.R.: Based microfluidic point-of-care diagnostic devices. Lab. Chip 13, 2210–2251 (2013).Google Scholar
64. Veerubhotla, R., Bandopadhyay, A., Das, D., and Chakraborty, S.: Instant power generation from an air-breathing paper and pencil based bacterial bio-fuel cell. Lab. Chip 15, 2580–2583 (2015).Google Scholar
65. Zhang, L., Zhou, M., Wen, D., Bai, L., Lou, B., and Dong, S.: Small-size biofuel cell on paper. Biosens. Bioelectron. 35, 155–159 (2012).Google Scholar
66. Shitanda, I., Kato, S., Hoshi, Y., Itagaki, M., and Tsujimura, S.: Flexible and high-performance paper-based biofuel cells using printed porous carbon electrodes. Chem. Commun. 49, 11110–11112 (2013).Google Scholar
67. Desselberger, U.: Emerging and re-emerging infectious diseases. J. Infect. 40, 3–15 (2000).Google Scholar
68. Cui, X. and Boland, T.: Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30, 6221–6227 (2009).Google Scholar
69. Martinez, A.W., Phillips, S.T., Carrilho, E., Thomas, S.W. III, Sindi, H., and Whitesides, G.M.: Simple telemedicine for developing regions: camera phones and paper-based microfluidic devices for real-time, off-site diagnosis. Anal. Chem. 80, 3699–3717 (2008).Google Scholar
70. Srimongkon, T., Ishida, T., Igarashi, K., and Enomae, T.: Development of a bacterial culture system using a paper platform to accommodate media and an ink-jet printing to dispense bacteria. Am. J. Biochem. Biotechnol. 10, 81–87 (2014).Google Scholar
71. Marciano, F., Lima-Oliveira, D., Da-Silva, N., Diniz, A., Corat, E., and Trava-Airoldi, V.: Antibacterial activity of DLC films containing TiO 2 nanoparticles. J. Colloid Interface Sci. 340, 87–92 (2009).Google Scholar
72. Zhang, L., Jiang, Y., Ding, Y., Daskalakis, N., Jeuken, L., Povey, M., O'Neill, A.J., and York, D.W.: Mechanistic investigation into antibacterial behaviour of suspensions of ZnO nanoparticles against E. coli. J. Nanopart. Res. 12, 1625–1636 (2010).Google Scholar
73. Tankhiwale, R. and Bajpai, S.: Preparation, characterization and antibacterial applications of ZnO-nanoparticles coated polyethylene films for food packaging. Colloids Surf. B 90, 16–20 (2012).CrossRefGoogle ScholarPubMed
74. Seil, J.T. and Webster, T.J.: Reduced Staphylococcus aureus proliferation and biofilm formation on zinc oxide nanoparticle PVC composite surfaces. Acta Biomater. 7, 2579–2584 (2011).CrossRefGoogle ScholarPubMed
75. Brayner, R., Ferrari-Iliou, R., Brivois, N., Djediat, S., Benedetti, M.F., and Fiévet, F.: Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett. 6, 866–870 (2006).Google Scholar
76. Choi, G. and Choi, S.: Monitoring electron and proton diffusion flux through three-dimensional, paper-based, variable biofilm and liquid media layers. Analyst 140, 5901–5907 (2015).Google Scholar
77. Azam, A., Ahmed, A.S., Oves, M., Khan, M.S., Habib, S.S., and Memic, A.: Antimicrobial activity of metal oxide nanoparticles against gram-positive and gram-negative bacteria: a comparative study. Int. J. Nanomed. 7, 6003 (2012).CrossRefGoogle ScholarPubMed
78. Pal, S., Tak, Y.K., and Song, J.M.: Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl. Environ. Microbiol. 73, 1712–1720 (2007).CrossRefGoogle ScholarPubMed
79. Sondi, I. and Salopek-Sondi, B.: Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for gram-negative bacteria. J. Colloid Interface Sci. 275, 177–182 (2004).Google Scholar
80. Díez, I., Eronen, P., Österberg, M., Linder, M.B., Ikkala, O., and Ras, R.H.: Functionalization of nanofibrillated cellulose with silver nanoclusters: fluorescence and antibacterial activity. Macromol. Biosci. 11, 1185–1191 (2011).CrossRefGoogle ScholarPubMed
81. Baruah, S., Jaisai, M., Imani, R., Nazhad, M.M., and Dutta, J.: Photocatalytic paper using zinc oxide nanorods. Sci. Technol. Adv. Mater. 11, 055002 (2010).Google Scholar
82. Ghule, K., Ghule, A.V., Chen, B.-J., and Ling, Y.-C.: Preparation and characterization of ZnO nanoparticles coated paper and its antibacterial activity study. Green Chem. 8, 1034–1041 (2006).Google Scholar
83. Pinto, R.J., Marques, P.A., Neto, C.P., Trindade, T., Daina, S., and Sadocco, P.: Antibacterial activity of nanocomposites of silver and bacterial or vegetable cellulosic fibers. Acta Biomater. 5, 2279–2289 (2009).Google Scholar
84. Martins, N.C., Freire, C.S., Pinto, R.J., Fernandes, S.C., Neto, C.P., Silvestre, A.J., Causio, J., Baldi, G., Sadocco, P., and Trindade, T.: Electrostatic assembly of Ag nanoparticles onto nanofibrillated cellulose for antibacterial paper products. Cellulose 19, 1425–1436 (2012).Google Scholar
85. Gottesman, R., Shukla, S., Perkas, N., Solovyov, L.A., Nitzan, Y., and Gedanken, A.: Sonochemical coating of paper by microbiocidal silver nanoparticles. Langmuir 27, 720–726 (2011).CrossRefGoogle ScholarPubMed
86. Ryan, M.J. and Smith, D.: Cryopreservation and freeze-drying of fungi employing centrifugal and shelf freeze-drying. Methods Mol. Biol. 368, 127–140 (2007).Google Scholar
87. Michaelsen, A., Pinzari, F., Ripka, K., Lubitz, W., and Piñar, G.: Application of molecular techniques for identification of fungal communities colonising paper material. Int. Biodeterior. Biodegrad. 58, 133–141 (2006).Google Scholar
88. Ben-Amotz, A., Fishler, R., and Schneller, A.: Chemical composition of dietary species of marine unicellular algae and rotifers with emphasis on fatty acids. Mar. Biol. 95, 31–36 (1987).CrossRefGoogle Scholar
89. Yen, H.W., Hu, I.C., Chen, C.Y., Ho, S.H., Lee, D.J., and Chang, J.S.: Microalgae-based biorefinery—from biofuels to natural products. Bioresour. Technol. 135, 166–174 (2013).Google Scholar
90. Liu, W., Dechev, N., Foulds, I.G., Burke, R., Parameswaran, A., and Park, E.J.: A novel permalloy based magnetic single cell micro array. Lab. Chip 9, 2381–2390 (2009).Google Scholar
91. Lindstrom, S. and Andersson-Svahn, H.: Miniaturization of biological assays—overview on microwell devices for single-cell analyses. Biochim. Biophys. Acta 1810, 308–316 (2011).Google Scholar
92. Khanna, S.: Microbiota replacement therapies: innovation in gastrointestinal care. Clin. Pharmacol. Ther. 103, 102–111 (2017).Google Scholar